Endocrinology and Metabolism

Original Articles

Thyroid
Hashimoto Thyroiditis and Mortality in Patients with Differentiated Thyroid Cancer: The National Epidemiologic Survey of Thyroid Cancer in Korea and Meta-Analysis: Injung Yang, Jae Myung Yu, Hye Soo Chung, Yoon Jung Kim, Yong Kyun Roh, Min Kyu Choi, Sung-ho Park, Young Joo Park, Shinje Moon; Endocrinol Metab. 2024;39(1):140-151. Published online January 3, 2024; DOI: https://doi.org/10.3803/EnM.2023.1748

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Abstract PDF Supplementary Material PubReader ePub: Background
Many studies have shown that Hashimoto’s thyroiditis (HT) acts as a protective factor in differentiated thyroid cancer (DTC), but little is known about its effects on mortality. Therefore, this study was performed to reveal the prognosis of HT on mortality in patients with DTC.
Methods
This study included two types of research results: retrospective cohort study using the National Epidemiologic Survey of Thyroid cancer (NEST) in Korea and meta-analysis study with the NEST data and eight selected studies.
Results
Of the 4,398 patients with DTC in NEST, 341 patients (7.8%) died during the median follow-up period of 15 years (interquartile range, 12.3 to 15.6). Of these, 91 deaths (2.1%) were related to DTC. HT was associated with a smaller tumor size and less aggressive DTC. In Cox regression analysis after adjusting for age and sex, patients with HT showed a significantly lower risk of all-cause death (hazard ratio [HR], 0.71; 95% confidence interval [CI], 0.52 to 0.96) and DTC-related death (HR, 0.33; 95% CI, 0.14 to 0.77). The analysis with inverse probability of treatment weight data adjusted for age, sex, and year of thyroid cancer registration showed similar association. The meta-analysis showed that patients with HT showed a lower risk of all-cause mortality (risk ratio [RR], 0.24; 95% CI, 0.13 to 0.47) and thyroid cancer-related mortality (RR, 0.23; 95% CI, 0.13 to 0.40) in comparison with patients without HT.
Conclusion
This study showed that DTC co-presenting with HT is associated with a low risk of advanced DTC and presents a low risk for all-cause and DTC-related death.

Thyroid
Immunoglobulin G4-Related Thyroid Disease: A Single-Center Experience and Literature Review: Meihua Jin, Bictdeun Kim, Ahreum Jang, Min Ji Jeon, Young Jun Choi, Yu-Mi Lee, Dong Eun Song, Won Gu Kim; Endocrinol Metab. 2022;37(2):312-322. Published online April 25, 2022; DOI: https://doi.org/10.3803/EnM.2021.1318

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Background
Immunoglobulin G4 (IgG4)-related disease is an entity that can involve the thyroid gland. The spectrum of IgG4-related thyroid disease (IgG4-RTD) includes Hashimoto thyroiditis (HT) and its fibrotic variant, Riedel thyroiditis, as well as Graves’ disease. The early diagnosis of IgG4-RTD is important because it is a medically treatable disease, and a delay in the diagnosis might result in unnecessary surgery. We present a case series of IgG4-RTD with a review of the literature.
Methods
We retrospectively reviewed the clinical presentation and the radiological and pathological findings of patients diagnosed with IgG4-RTD between 2017 and 2021 at a tertiary medical center in Korea. We also conducted a literature review of IgG4-RTD.
Results
Five patients were diagnosed with IgG4-RTD during the study period. The patients’ age ranged from 31 to 76 years, and three patients were men. Most patients visited the clinic for a neck mass, and hypoechogenic nodular lesions were observed on neck ultrasonography. Three patients had IgG4 HT, and two patients had IgG4 Riedel thyroiditis. All patients developed hypothyroidism that necessitated L-thyroxine replacement. The diagnosis of IgG4-RTD was confirmed after a pathological examination of the surgical specimen in the first two cases. However, the early diagnosis was possible after a core needle biopsy in three clinically suspected patients.
Conclusion
The diagnosis of IgG4-RTD requires clinical suspicion combined with serology and histological analyses using IgG4 immunostaining. The early diagnosis of IgG4-RTD is difficult; thus, biopsy with IgG4 immunostaining and serum IgG4 measurements will help diagnose patients suspected of having IgG4-RTD.

Citations

Citations to this article as recorded by

Are sonographic characteristics of Hashimoto’s thyroiditis related with immunologic parameters? A cross-sectional study
K. Kenarlı, A. B. Bahçecioğlu, Ö. B. Aksu, S. Güllü
Journal of Endocrinological Investigation.2024;[Epub] CrossRef
Reshaping the Concept of Riedel’s Thyroiditis into the Larger Frame of IgG4-Related Disease (Spectrum of IgG4-Related Thyroid Disease)
Mara Carsote, Claudiu Nistor
Biomedicines.2023; 11(6): 1691. CrossRef

Thyroid
Programmed Cell Death-Ligand 1 (PD-L1) gene Single Nucleotide Polymorphism in Graves’ Disease and Hashimoto’s Thyroiditis in Korean Patients: Jee Hee Yoon, Min-ho Shin, Hee Nam Kim, Wonsuk Choi, Ji Yong Park, A Ram Hong, Hee Kyung Kim, Ho-Cheol Kang; Endocrinol Metab. 2021;36(3):599-606. Published online June 2, 2021; DOI: https://doi.org/10.3803/EnM.2021.965

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Background
Programmed cell death-ligand 1 (PD-L1) has an important role in regulating immune reactions by binding to programmed death 1 (PD-1) on immune cells, which could prevent the exacerbation of autoimmune thyroid disease (AITD). The aim of this study was to evaluate the association of PD-L1 polymorphism with AITD, including Graves’ disease (GD) and Hashimoto’s thyroiditis (HT).
Methods
A total of 189 GD patients, 234 HT patients, and 846 healthy age- and sex-matched controls were enrolled in this study. We analyzed PD-L1 single nucleotide polymorphism (SNP) (rs822339) and investigated the associations with clinical disease course and outcome.
Results
Genotype frequency at the PD-L1 marker RS822339 in GD (P=0.219) and HT (P=0.764) patients did not differ from that among healthy controls. In patients with GD, the A/G or G/G genotype group demonstrated higher TBII titer (20.6±20.5 vs. 28.0± 25.8, P=0.044) and longer treatment duration (39.0±40.4 months vs. 62.4±65.0 months, P=0.003) compared to the A/A genotype group. Among patients in whom anti-thyroid peroxidase (TPO) antibody was measured after treatment of GD, post-treatment antiTPO positivity was higher in the A/G or G/G genotype group compared to the A/A genotype group (48.1% vs. 69.9%, P=0.045). Among patients with HT, there was no significant difference of anti-TPO antibody positivity (79.4% vs. 68.6%, P=0.121), anti-thyroglobulin antibody positivity (80.9% vs. 84.7%, P=0.661), or development to overt hypothyroidism (68.0% vs. 71.1%, P=0.632) between the A/A genotype group and the A/G or G/G genotype group.
Conclusion
The genotype frequency of PD-L1 (rs822339) is not different in patients with AITD compared with healthy controls. The intact PD-1/PD-L1 pathway in GD and HT might be important to maintain chronicity of AITD by protecting immune tolerance. However, the PD-L1 SNP could be associated with difficulty in achieving remission in patients with GD, which may be helpful to predict the possibility of longer treatment. Further studies are required to investigate the complex immune tolerance system in patients with AITD.

Citations

Citations to this article as recorded by

Synergistic effects of BTN3A1, SHP2, CD274, and STAT3 gene polymorphisms on the risk of systemic lupus erythematosus: a multifactorial dimensional reduction analysis
Yang-Yang Tang, Wang-Dong Xu, Lu Fu, Xiao-Yan Liu, An-Fang Huang
Clinical Rheumatology.2024; 43(1): 489. CrossRef
Relationship between CD274 gene polymorphism and systemic lupus erythematosus risk in a Chinese Han population
Lu‐Qi Yang, Zhen Qin, Lu Fu, Wang‐Dong Xu
International Journal of Rheumatic Diseases.2024;[Epub] CrossRef

Clinical Study
Mechanisms of the Impact of Hashimoto Thyroiditis on Papillary Thyroid Carcinoma Progression: Relationship with the Tumor Immune Microenvironment: Oksana Sulaieva, Olena Chernenko, Oleksiy Selesnov, Oleksandr Nechay, Oleksandr Maievskyi, Tetyana Falalyeyeva, Nazarii Kobyliak, Olena Tsyryuk, Yurii Penchuk, Dmytro Shapochka; Endocrinol Metab. 2020;35(2):443-455. Published online June 24, 2020; DOI: https://doi.org/10.3803/EnM.2020.35.2.443

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Background
The relationship between Hashimoto thyroiditis (HT) and papillary thyroid carcinoma (PTC) remains uncertain. We assessed the impact of HT on the tumor immune microenvironment (TIME) in PTC.
Methods
Thirty patients with PTC (group 1) and 30 patients with PTC and HT (group 2) were enrolled in this pilot study. The distribution and number of CD8+ lymphocytes, plasma cells (CD138+), regulatory T cells (forkhead box P3 [FOXP3+)], mast cell tryptase (MCT+), and M2 macrophages (CD163+) were evaluated. To test the hypothesis that HT impacts PTC development via signal transducer and activator of transcription 6 (STAT6) activation and M2 macrophage polarization, we investigated STAT6 expression in tumor and stromal cells. We also evaluated vascular endothelial growth factor (VEGF) expression by lymph node metastasis (LNM) status.
Results
TIME showed significant between-group differences. Group 1 patients demonstrated immune desert or immune-excluded immunophenotypes, while an inflamed phenotype with more CD8+ cells (P<0.001) predominated in group 2. Immune-excluded TIME was associated with the highest LNM rate. In PTC, LNM was associated with more numerous CD163+ cells. Moreover, LNM in group 1 was associated with increased numbers of mast cells peritumorally and FOXP3+ cells intratumorally and peritumorally. Group 2 demonstrated higher STAT6 but not higher VEGF expression in tumor cells. High VEGF expression was associated with LNM regardless of HT status.
Conclusion
Concomitant HT impacted PTC signaling via STAT6 and TIME by increasing the number of CD8+ cells. LNM is associated with increases in CD163+ cells and VEGF expression in PTC, whereas HT affected LNM through different mechanisms.

Citations

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Thyroid
Associations between Hashimoto Thyroiditis and Clinical Outcomes of Papillary Thyroid Cancer: A Meta-Analysis of Observational Studies: Shinje Moon, Hye Soo Chung, Jae Myung Yu, Hyung Joon Yoo, Jung Hwan Park, Dong Sun Kim, Young Joo Park; Endocrinol Metab. 2018;33(4):473-484. Published online November 30, 2018; DOI: https://doi.org/10.3803/EnM.2018.33.4.473

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Abstract PDF Supplementary Material PubReader ePub

Background

Epidemiological studies have suggested an association between Hashimoto thyroiditis (HT) and papillary thyroid cancer (PTC) development. Other studies, however, have reported a protective role of HT against PTC progression. Through this updated meta-analysis, we aimed to clarify the effects of HT on the progression of PTC.

Methods

We searched citation databases, including PubMed and Embase, for relevant studies from inception to September 2017. From these studies, we calculated the pooled odds ratios (ORs) of clinicopathologic features and the relative risk (RR) of PTC recurrence with 95% confidence intervals (CIs) using the Mantel-Haenszel method. Additionally, the Higgins I² statistic was used to test for heterogeneity.

Results

The meta-analysis included 71 published studies with 44,034 participants, among whom 11,132 had HT. We observed negative associations between PTC with comorbid HT and extrathyroidal extension (OR, 0.74; 95% CI, 0.68 to 0.81), lymph node metastasis (OR, 0.82; 95% CI, 0.72 to 0.94), distant metastasis (OR, 0.49; 95% CI, 0.32 to 0.76), and recurrence (RR, 0.50; 95% CI, 0.41 to 0.61).

Conclusion

In this meta-analysis, PTC patients with HT appeared to exhibit more favorable clinicopathologic characteristics and a better prognosis than those without HT.

Citations

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Review Articles

Thyroid
Genome-Wide Association Studies of Autoimmune Thyroid Diseases, Thyroid Function, and Thyroid Cancer: Yul Hwangbo, Young Joo Park; Endocrinol Metab. 2018;33(2):175-184. Published online June 21, 2018; DOI: https://doi.org/10.3803/EnM.2018.33.2.175

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Thyroid diseases, including autoimmune thyroid diseases and thyroid cancer, are known to have high heritability. Family and twin studies have indicated that genetics plays a major role in the development of thyroid diseases. Thyroid function, represented by thyroid stimulating hormone (TSH) and free thyroxine (T4), is also known to be partly genetically determined. Before the era of genome-wide association studies (GWAS), the ability to identify genes responsible for susceptibility to thyroid disease was limited. Over the past decade, GWAS have been used to identify genes involved in many complex diseases, including various phenotypes of the thyroid gland. In GWAS of autoimmune thyroid diseases, many susceptibility loci associated with autoimmunity (human leukocyte antigen [HLA], protein tyrosine phosphatase, non-receptor type 22 [PTPN22], cytotoxic T-lymphocyte associated protein 4 [CTLA4], and interleukin 2 receptor subunit alpha [IL2RA]) or thyroid-specific genes (thyroid stimulating hormone receptor [TSHR] and forkhead box E1 [FOXE1]) have been identified. Regarding thyroid function, many susceptibility loci for levels of TSH and free T4 have been identified through genome-wide analyses. In GWAS of differentiated thyroid cancer, associations at FOXE1, MAP3K12 binding inhibitory protein 1 (MBIP)-NK2 homeobox 1 (NKX2-1), disrupted in renal carcinoma 3 (DIRC3), neuregulin 1 (NRG1), and pecanex-like 2 (PCNXL2) have been commonly identified in people of European and Korean ancestry, and many other susceptibility loci have been found in specific populations. Through GWAS of various thyroid-related phenotypes, many susceptibility loci have been found, providing insights into the pathogenesis of thyroid diseases and disease co-clustering within families and individuals.

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Thyroid
Clinical Update in Aspects of the Management of Autoimmune Thyroid Diseases: Duncan J. Topliss; Endocrinol Metab. 2016;31(4):493-499. Published online December 20, 2016; DOI: https://doi.org/10.3803/EnM.2016.31.4.493

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Abstract PDF PubReader

Aspects of autoimmune thyroid disease updated in this review include: immunoglobulin G4 (IgG4)-related thyroid disease (Riedel's thyroiditis, fibrosing variant of Hashimoto's thyroiditis, IgG4-related Hashimoto's thyroiditis, and Graves' disease with elevated IgG4 levels); recent epidemiological studies from China and Denmark indicating that excess iodine increases the incidence of Hashimoto's thyroiditis and hypothyroidism; immunomodulatory agents (ipilimumab, pembrolizumab, nivolumab) activate immune response by inhibiting T-cell surface receptors which down-regulate immune response, i.e., cytotoxic T-lymphocyte antigen 4 and programmed cell death protein 1 pathways; alemtuzumab is a humanised monoclonal antibody to CD52 which causes immune depletion and thyroid autoimmune disease especially Graves' hyperthyroidism; small molecule ligand (SML) agonists which activate receptors, SML neutral antagonists, which inhibit receptor activation by agonists, and SML inverse agonists which inhibit receptor activation by agonists and inhibit constitutive agonist independent signaling have been identified. SML antagonism of thyroid-stimulating hormone-receptor stimulatory antibody could treat Graves' hyperthyroidism and Graves' ophthalmopathy; and thyroxine treatment of subclinical hypothyroidism can produce iatrogenic subclinical hyperthyroidism with the risk of atrial fibrillation and osteoporosis. The increased risk of harm from subclinical hyperthyroidism may be stronger than the potential benefit from treatment of subclinical hypothyroidism.

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Thyroid
Recent Advances in Autoimmune Thyroid Diseases: Won Sang Yoo, Hyun Kyung Chung; Endocrinol Metab. 2016;31(3):379-385. Published online August 26, 2016; DOI: https://doi.org/10.3803/EnM.2016.31.3.379

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Autoimmune thyroid disease (AITD) includes hyperthyroid Graves disease, hypothyroid autoimmune thyroiditis, and subtle subclinical thyroid dysfunctions. AITD is caused by interactions between genetic and environmental predisposing factors and results in autoimmune deterioration. Data on polymorphisms in the AITD susceptibility genes, related environmental factors, and dysregulation of autoimmune processes have accumulated over time. Over the last decade, there has been progress in the clinical field of AITD with respect to the available diagnostic and therapeutic methods as well as clinical consensus. The updated clinical guidelines allow practitioners to identify the most reasonable and current approaches for proper management. In this review, we focus on recent advances in understanding the genetic and environmental pathogenic mechanisms underlying AITD and introduce the updated set of clinical guidelines for AITD management. We also discuss other aspects of the disease such as management of subclinical thyroid dysfunction, use of levothyroxine plus levotriiodothyronine in the treatment of autoimmune hypothyroidism, risk assessment of long-standing antithyroid drug therapy in recurrent Graves' hyperthyroidism, and future research needs.

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Case Report

Thyroid
Co-Occurrence of Papillary Thyroid Carcinoma and Mucosa-Associated Lymphoid Tissue Lymphoma in a Patient with Long-Standing Hashimoto Thyroiditis: Yoon Jeong Nam, Bo Hyun Kim, Seong Keun Lee, Yun Kyung Jeon, Sang Soo Kim, Woo Jin Jung, Dong Hwahn Kahng, In Ju Kim; Endocrinol Metab. 2013;28(4):341-345. Published online December 12, 2013; DOI: https://doi.org/10.3803/EnM.2013.28.4.341

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Papillary thyroid carcinoma (PTC) is a common affliction of the thyroid gland, accounting for 70% to 80% of all thyroid cancers, whereas mucosa-associated lymphoid tissue (MALT) lymphoma of the thyroid gland is uncommon. The simultaneous occurrence of both malignancies is extremely rare. We report the case of a patient with both PTC and MALT lymphoma in the setting of Hashimoto thyroiditis. An 81-year-old female patient was first admitted with goiter and hoarseness, which was attributed to an ultrasonographic thyroid nodule. Subsequent fine-needle aspirate, interpreted as suspicious of papillary thyroid cancer, prompted total thyroidectomy. MALT lymphoma was an incidental postsurgical finding, coexisting with PTC in the setting of Hashimoto thyroiditis. Although the development of MALT lymphoma is very rare, patients with longstanding Hashimoto thyroiditis should undergo careful surveillance for both malignancies.

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Original Article

Predictive Factors for Incidental Contralateral Carcinoma in Patients with Unilateral Micropapillary Thyroid Carcinoma.: Jung Eun Huh, Sang Soo Kim, Ji Hyun Kang, Bo Gwang Choi, Byung Joo Lee, Jin Choon Lee, Yun Kyung Jeon, Bo Hyun Kim, Soo Geun Wang, Yong Ki Kim, In Joo Kim; Endocrinol Metab. 2012;27(3):194-199. Published online September 19, 2012; DOI: https://doi.org/10.3803/EnM.2012.27.3.194

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BACKGROUND
Whether thyroid lobectomy alone is a sufficient treatment for papillary thyroid microcarcinoma (PTMC) remains controversial. The aim of this study is to evaluate the predictive factors for incidental contralateral carcinoma in patients confirmed of unilateral PTMC preoperatively. METHODS: Between January 2007 and December 2009, 393 patients underwent thyroid surgery for unifocal and unilateral PTMC preoperatively at Pusan National University Hospital. A total thyroidectomy with central neck dissection was routinely performed for these patients during this study period. RESULTS: Among the 393 cases in the cohort, 77 patients (19.6%) had incidental PTMC in the contralateral lobe. In patients with incidental contralateral carcinoma, there was higher prevalence in extrathyroid extension, occult ipsilateral carcinoma, pathologic Hashimoto's thyroiditis, and central lymph node metastasis compared to those without contralateral carcinoma. The mean tumor size also increased in patients with contralateral carcinoma. Multivariate logistic regression showed that extrathyroid extension (P = 0.049), occult ipsilateral carcinoma (P < 0.001), pathologic Hashimoto's thyroiditis (P = 0.038), and central lymph node metastasis (P = 0.002) were predictive factors for incidental contralateral carcinoma. CONCLUSION: In conclusion, multifocality in the ipsilateral lobe, central lymph node metastasis, extrathyroid extension, and Hashimoto's thyroiditis is associated with the presence of contralateral carcinoma. Thus, if these factors are found by preoperative and/or postoperative evaluation, total thyroidectomy or completion thyroidectomy is necessary for the treatment of PTMC.

Citations

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Extent of surgery did not affect recurrence during 7‐years follow‐up in papillary thyroid cancer sized 1‐4 cm: Preliminary results
Min Joo Kim, Myung‐Chul Lee, Guk Haeng Lee, Hoon Sung Choi, Sun Wook Cho, Su‐jin Kim, Kyu Eun Lee, Young Joo Park, Do Joon Park
Clinical Endocrinology.2017; 87(1): 80. CrossRef

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